L

Historical introduction: on widely foragingfor Kalahari lizards

RAYMOND B. HUEYDepartment oj Zoology, University oj Washington

ERIC R. PIANKADepartment oJZoology, University oJ Texas

This book shows that the field of foraging biology of reptiles is alive and well.We find this exciting, as we've been interested in this field for four decades. Nodoubt for that reason, we've been asked to describe the history of our thinkingabout foraging modes. How did we become involved? What were some of thesalient experiences we had, and what insights of others helped channel ourthinking?

When Eric began studying US desert lizards in the early 1960s, he immedi-ately noted that the teiid Cnemidophorus moved much more than did all speciesof iguanids. This lizard world was clearly dichotomous in terms of foragingbehavior. In his 1966 paper in Ecology, Eric coined the terms "sit-and-wait"(hereafter SW) and "widely foraging" (hereafter WF) to characterize thesedifferent behaviors.

Ray's interest in foraging behavior evolved independently about the sametime. As an undergraduate at UC Berkeley in the spring of 1965, he tookNatural History of the Vertebrates (taught by R. C. Stebbins and others).Students were required to do a field project: Ray studied the feeding behavior ofgreat blue herons. In his term paper (Huey, 1965), he noted that herons "... usetwo distinct types of hunting whether on land or in water - stalking andstill hunting." Further, he observed that herons hunting in estuaries willswitch to "still hunting" when the tide is coming in, letting the movingwater bring food to the birds. Thus the dichotomy of foraging behaviors heobserved within a species was exactly the same as what Eric had observedbetween species!

In 1966 Eric headed to Australia on a postdoc, and in 1967 Ray startedgraduate school at the University of Texas (UT). Ray was fascinated by Eric's work(and also byTom Schoener's) on species diversity and competition in lizards,and their studies inspired him to do his MA thesis on competitive relations ofgeckos from the Sechura Desert in Peru. When he read Eric's paper (Pianka,

Lizard Ecology: The Evolutionary Consequences of Foraging Mode, ed. S. M. Reilly, L. D. McBrayerand D. B. Miles. Published by Cambridge University Press. © Cambridge University Press 2007.

1966), he found that his own observations on herons fit in neatly within Eric'sconcept, terminology, and ideas on foraging mode.

By a remarkable and fortuitous coincidence, Eric joined the faculty at UT infall 1968. Eric and Ray became instant friends and intellectual soul mates,given their many mutual interests (in lizards, foraging mode, and far-awaydeserts). The next winter Eric received an NSF grant to study species diversityof lizards in the Kalahari; and he hired Ray and Larry Coons to work as hisfield assistants beginning in November 1969.

Eric arrived in the Kalahari a month later, and the three of us spent twowonderful months observing and collecting lizards in the Kalahari and Namib,drinking non-hot beer, and avoiding lions, leopards, scorpions, puff adders,and cape cobras. We no longer recall who first noticed that different species oflacertids were either WF or SW - given our histories, that pattern was prob-ably immediately obvious to us both!

In any case, Ray had two experiences later on that trip that crystallized ourthinking on the ecological significance of foraging mode. First, he realizedthat we ourselves were widely foraging predators on lizards; and that ourforaging behavior must not only increase our encounter rates with lizards,but also influence the kinds oflizards we'd encounter. For example, our WFmovements would necessarily increase our encounters with sedentary SWlizards. Second, Ray remembers walking one day along a sand ridge, wonder-ing why we always found a WF paired with a SW lizard in a given habitat(e.g. Meroles suborbitalis with Pedioplanis namaquensis on white interdunalstreet sands, and Pedioplanis lineoocellata with Heliobolus lugubris on thered sand ridges), but never two WF species or two SW species paired in ahabitat (see Pianka et al., 1979). Although this pairing could obviously havehappened by chance, Ray wondered whether foraging mode might in factinfluence the kinds of prey a lizard would encounter. If so, differences inforaging mode might reduce dietary overlap and facilitate spatial overlap.As soon as he posed these issues, he predicted that WF lizards shouldencounter more patchily distributed and sedentary prey (e.g. termites),whereas SW lizards should encounter mainly moving prey. To our delight,this prediction was validated when we analyzed the dietary data (Huey andPianka, 1981).

Yet another important insight emerged from our Kalahari peregrinations.All too frequently we stepped on horned adders (Bitis caudalis), which hunt byburying themselves (except for their eyes) in the sand, catching unsuspectinglizards that happen to wander by. These vipers responded viciously to ourtransgressions by "leaping" out of the sand, striking at our feet and legs. Notsurprisingly, our initial response was always that of sheer terror; and we were

inspired to invent the 'Kalahari two-step,' an intensely evasive dance that hascuriously never caught on with the general public. In any case, once ouradrenalin titers dropped, we recognized that these vipers were archetypal(and arch-villain) SW predators.

Ray later made a related, but critical, observation one day near Tsabong,Botswana, while watching a secretary bird foraging for lizards. It would walkbriskly up to a bush and suddenly raise its wings, startling any nearby lizard(most likely a SW species), which it then grabbed as the lizard fled. Thus bothhorned adders and secretary birds preyed on lizards, but did so with polaropposite foraging modes. These differences were striking to us, and we pre-dicted that these two predators should eat different species of lizard. Fittingneatly with our expectations, SW sand vipers preyed relatively heavily on WFlizards, whereas WF secretary birds caught disproportionate numbers ofSW lizards. These field observations - and Don Broadley's (1972) remarkabledietary data - led us to propose the idea of crossovers in foraging modebetween trophic levels as well as to argue that models of foraging mode neededto incorporate interactions among multiple trophic levels, not just betweenpredator and prey (Huey and Pianka, 1981).

Ray flew back to Austin in late November 1970, and he used the long flightto begin synthesizing our ideas on the ecology of foraging mode. He scribbled·these on the back of airline non-slip placemats. Over the next few weeks, wespent many fruitful hours huddled over those placemats; and we talked andtalked until our ecological correlates began to gel.

Nevertheless, our foraging mode project soon went into torpor. OtherKalahari projects (and Ray's thesis work on thermoregulation) took prece-dence. But one important realization that became increasingly apparent to usduring this period was the comparative beauty of the Kalahari system -namely, that close relatives differed in foraging mode. That was not at all thecase in the North American deserts, where any observed difference in ecologybetween SW vs. WF species might reflect foraging mode, or it might merelyreflect long separate phylogenetic histories (iguanids vs. teiids), or both (Hueyand Pianka, 1981; Huey and Bennett, 1986, p. 85). One couldn't easily tellwhich (but see Anderson and Karasov, 1988).

Another reason for delaying publication was simply that we had no quanti-tative data on foraging movements. So on a return trip in 1975-6 generouslysponsored by the National Geographic Society, we (and Carolyn Cavalier)quantified various aspects of foraging behavior of our lacertids among otherstudies (Huey and Pianka, 1981; Huey et al., 1983). We measured time spentmoving and number of moves per minute for six species of lacertid, two of

which were SW and four WF foragers (see also Cooper and Whiting, 1999).With these data, we finally had all of the elements in hand for a paper.

About the same time, many others were working on related aspects offoraging mode in herps. Bennett and Gorman (1979) and Anderson andKarasov (1981) had estimated metabolic costs of different foraging modes.Bennett and Licht (1973) and Ruben (1976, 1977) explored physiologicaland morphological differences in reptiles with different foraging modes. Vittand Congdon (1978) drew attention to striking differences in morphology andreproductive effort, and proposed that relative clutch mass, body shape, andforaging mode were co-evolved characters. Regal (1978) argued that WFlizards might have enhanced learning and memory, as well as larg~r brains.Cathy Toft (1981) noted a number of parallels in frogs, and added the fasci-nating observation that WF tropical anurans are typically very poisonous.Cathy's observation was especially interesting to us, because we had discov-ered that the juveniles of one of our WF lacertids (Heliobolus lugubris) mim-icked a very noxious "oogpister" beetle (Huey and Pianka, 1977; Schmidt,2004). WF animals are of course relatively conspicuous to visually huntingpredators, and thus poisons and mimicry may be relatively common ways ofreducing predation on such species.

Foraging mode of herps was obviously a field whose time had come by the1970s! It was clearly and simultaneously attracting the attention of diverseherpetologists. So when we finally put our thoughts down on paper (piankaet al., 1979); Huey and Pianka, 1981) we drew on the insights of many others,not just our own. Our synthetic debt to all is clearly evident in Table 8 in our1981 paper.

Huey returned once more to the Kalahari in 1981-2 to investigate physio-logical correlates of foraging mode. This time he worked with three top-flight physiological ecologists (AI Bennett, Henry John-Alder, and KenNagy). They found that WF vs. SW species differed in locomotor capacity(acceleration, maximal speed, and stamina) (Huey et al., 1984; but see Perry,1999), differed in field metabolic rates and feeding rates (Nagy et al., 1984),and also differed in some (but not all) lower-level physiological traits (Bennettet al., 1984).

Finally, Huey and Bennett (1986) were invited to contribute a chapter to avolume on predator-prey relationships in lower vertebrates (Feder andLauder, 1986). This was right at the beginning of the "Felsenstein era" ofcomparative biology, marked by Felsenstein's remarkable, now classic, 1985paper. We were already well aware of the suitability of lacertids for compara-tive studies of foraging mode and had noted (Huey and Pianka, 1981, p. 991)that the close relationships of these lizards provided "a substantial measure of

control over phylogenetic and sensory differences." Huey and Bennett (1986)now took that a step further and speculated on the direction of evolutionarychange within this lineage. They used a crude phylogeny of the lacertids tosuggest that SW was derived in this group, and next explored various selectivefactors that might have favored this evolutionary transition. Improved phy-logenies (see, for example, Harris et al., 1998) and reconstructions in Perry(1999) and McBrayer (2004) seem to support the suggestion (Huey andBennett (1986) that SW is derived.

The two of us are rapidly approaching our academic dotage (but we're notthere yet!), and we take this opportunity to reflect on our own foraging-modework as well as add a few observations on current research in this field today.On a personal level, our Kalahari studies of foraging mode were great fun todo and had a big effect on our academic development. Those studies weregrowth experiences for us: in the process, we taught ourselves the criticalimportance of integrating field studies of behavior and ecology with labora-tory and field studies of physiology (energetics and locomotor capacity).Moreover, we taught ourselves the importance of conducting comparativestudies within an explicit phylogenetic context. We admit to some pride, ofcourse, in the continuing impact of our studies (Fig. AI, and this volume) and:those of others involved at the same time.

When we reflect on our old work, several things strike us as worth emphasizing.

YearFigure AI. Number of citations per year of Huey and Pianka (1981). Thecurve is a non-parametric super-smoother.

First, our experiences reinforce the often-forgotten view that novel ideascan emerge from seemingly trivial natural history observations of animals innature (Gans, 1978; Bartholomew, 1986; Greene, 1986, 2005). Who wouldhave ever guessed that so much work would evolve in part from Eric'sobservations of the movement patterns of North American lizards or ofRay's of great blue herons? Or who would have thought that our steppingon horned adders would inspire the arcane idea of trophic crossovers?

Second, our work with lacertids helped make us both keenly aware of theimportance of phylogeny and phylogenetic control in comparative biology. Thisis old news now, but it certainly was not in 1981 or even in 1986. In those "darkdays of ecology" (W. L. Hodges, personal communication), comparative studiesalmost invariably involved distant relatives (cf. Huey, 1987), were generallyrestricted to only two species (Garland and Adolph, 1994), and rarely consi-dered phylogeny (but see Greene and Burghardt, 1978!). Times have changed,and explicit phylogenetic approaches involving many species are now standard.

Third, we note that our paper is commonly viewed as advocating a strictlydichotomous view of foraging mode (Pietruszka, 1986; McLaughlin, 1989;Helfman, 1990). To be sure, we did emphasize the bimodality of foraging modein our lacertids. But what is often overlooked is that we explicitly discussedflexibility in foraging mode and its consequences and constraints (see alsoNorberg, 1977). To us, this is an area offoraging mode that remains severelyunderstudied (but see Dunham, 1981; Karasov and Anderson, 1984).

The flexibility offoraging mode is directly relevant to continuing attempts toquantify whether foraging modes are really dichotomous (vs. continuous)among species of lizards. Those analyses proceed by pooling data from differ-ent taxa with different habits and habitats into a single analysis, and thentesting for bimodality. In our view such approaches - though well motivatedand often statistically elegant - are weak comparative tests and in fact are.potentially biased in favor of a continuum of foraging modes. Why? Foragingmode isn't an invariant behavior but varies with the immediate environmentalconditions (Norberg, 1977; Huey and Pianka, 1981; Karasov and Anderson,1984). If that environmental sensitivity is general, then composite analyses ofmovement rates of diverse species that forage in habitats as different as temperate-zone deserts and tropical forests (or that forage on substrates as differentas ground or on branches; or that forage at different times) will necessarilyblur any potential divergence in foraging mode. Such comparisons may bemeaningful only when habit and habitat as well as phylogeny are controlled.

Moreover, Laurie Vitt (personal communication) has cautioned that forag-ing analyses that are based on movement rates must consider the context ofmovement (or lack thereof) - otherwise data can be misleading. For example,

some WF species periodically punctuate their active foraging and sit forextended periods to bask or to cool (Hillman, 1969; van Berkum et al.,1986). Conversely, males of some SW species start moving extensively duringthe breeding season (Pietruszka, 1986), but their movements are likely relatedto searching for mates, not food. By failing to consider the natural historycontext of movement, an incautious investigator quantifying movement of theabove species could grossly misrepresent true foraging rates.

To us, the proper way to address this issue is to select a single habitat andtaxonomic group as the unit for analysis, to appreciate the ecological context ofobserved movement patterns, and to assay whether the lizards in that habitathave dichotomous, continuous, or invariant foraging modes. Then to deter-mine generality for lizards, one would need to iterate that procedure throughadditional habitats and taxa and ultimately determine the proportion of casesshowing bimodality versus a continuum. We took a first step with Kalaharilacertids, but we are fully aware that seemingly limited variation in foragingbehavior within most other taxa (Perry, 1999; Vitt and Pianka, 2005) hindersor even precludes parallel analyses in most environments. Unfortunately,evolution hasn't always cooperated with the analytical needs of comparativebiologists (Huey, 1987)!

What's happened to our own interests since those wonderful days of ouryouth, foraging widely over the red dunes of the Kalahari? In his old age, Erichas switched from being a WF to a SW hunter oflizards. He notes that he can'thear or see as well as he once could, and that his bad leg can't support his newhuge mass as well as it could when he weighed only 140-155 pounds. So now hepit traps lizards, almost exclusively, except for monitor lizards, large ones ofwhich are too big to trap. But he is still avidly pursuing foraging mode. Withthe help of Bill Cooper and Kurt Schwenk, Pianka and Laurie Vitt recentlyachieved a synthesis of the history of evolutionary innovations that led to theevolution of widely foraging (Pianka and Vitt 2003; Vitt et al. 2003). Recently,they demonstrated that 28% of the variance in diets of 184 extant lizard speciesin 12 families from 4 continents can be attributed to the first split in squamatephylogeny 200Ma when Iguania and Scleroglossa split (Vitt and Pianka 2005).Iguanians retained ancestral traits including tongue prehension and ambushforaging, whereas scleroglossans switched from tongue prehension to jawprehension. This freed the tongue to evolve along new lines (Schwenk andWagner, 2001), ultimately leading to much keener vomerolfaction, which inturn promoted a more active lifestyle and facilitated a shift to wide foraging.

Rayon the other hand has largely moved away from the world oflizards andforaging biology. He claims to have good reasons for doing so (see Huey,1994), but many herpers no doubt see his departure as clear evidence of moral

deterioration and premature senility - what else could explain his evolutionarytransition to the worlds of fruit flies and mountain climbers? He still does fieldwork but is no longer a WF hunter of wily lizards in remote deserts - instead heis reduced to running a trap line and collecting piddly Drosophila on rotting,smelly banana baits. Perhaps this book will inspire him back into the fold.

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